A Common Digenetic Trematode of Fishes—

The Resources Agency of California Department of Fish and Game

A BIBLIOGRAPHY AND HOST LIST FOR THE YELLOW GRUB, CLINOSTOMUM MARGINATUM (RUDOLPBI, 18191,/ A COMMON DIGENETIC TREMATODE OF FISHES—/

LEE W. MILLER Region 5; Inland Fisheries—

SUMMARY

The yellow grub is distributed over most of North America. It is economically important in some commercial and sport fisheries because it renders fish undesirable for human consumption.

A check list of fish hosts shows that C. marginatum occurs in 15 families and 67 species of North American freshwater fishes.

Feasible methods of breaking the life cycle and controlling the parasite are not presently available for wide applica- tion.

1 /Submitted December 1966. Inland Fisheries Administrative Report No. 66-17. ./Now with Inland Fisheries Branch. 0 46 ... :.1 -3- INTRODUCTION

The yellow grub, Clinostomum marginatum, has economic importance in many fisheries. The metacercarial stage of this parasite ranges from t to i inch in length, and is most often found .under the skin or in the musculature of fishes. It is most evident to fishermen when cleaning their catch. Infested fish are esthetically undesirable for human consumption, and are often the cause of angler inquiries to conservation and public health agencies. Members of this genus have been reported as an aberrant parasite in man (Kamo, Ogiwo, and Hatsushika, 1962). This bibliography was compiled to provide a reference source on the ecology and hosts of C. marginatum.

ACKNOWLEDGMENTS

I am grateful to Dr.'.Carl L. Hubbs for the use of his extensive library for this research. I also thank the California Resources Agency Library staff for assistance in obtaining materials, and Richard Haley and Marvin J. Wballs for reviewing the manuscript.

TAXONOMY AND DISTRIBUTION

Clinostomum marginatuxa is a digenetic trematode of the Family Clinostomidae. A complete classification of the group may be found in Yamaguti (1958).

Osborn (1911) snirmarizes the early literature and lists many of the synonyms for the species. Nigrelli (1936) reviews some papers on the taxonomy of the genus. He considers C. marginatum (Rudolphi, 1619) synonymous with C. complanatum (Rudolphi, 1814) because of similar morphology, hosts, and geographical distribution. Price (1938) lists the two as synonyms.

The known zoogeography of this parasite is greatly extended, based on this synonymy. The metacercarial stage of C. marginatum has been reported in numerous fish parasite surveys throughout North America. Nigrelli (1936) reports its occurrence in fish from Central and South America. The distribution of C. complanatum, according to Yamaguti (1958) is cosmopolitan, having been re-ported in Europe, Australia, and Africa (Chapham, 1945), in addition to North America (Forney, 1955; MacLulich, 1943).

The evidence supporting the synonymy of C. complanatum and C. marginatum appears to be sufficient. The name Clinostomum complanatum (Rudolphi, 1814) precedes Clinostomum marginatum (Rudolphi, 1819), but C. marainatum has been commonly used in North America.

ECOLOGY

Life Cycle

The life cycle of the yellow grub was first described by Hunter and Hunter (1935b) and has since been summarized by Meyer (1954), Klaas (1963), Davis (1953), and others.

A brief outline of this cycle is shown in Figure 1. Although the life cycle of C. marginatum has been known since the work of Hunter and Hunter (1935b) the ecological conditions which contribute to infestation of fish populations are not well known.

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DEFINITIVE HOST FIRST INTERMEDIATE HOST

BIRDS Snails of the genus Helisoma

Great blue heron,.Ardea herodi4s, and other wading birds

Spo cyst and redial stages NLn small livers

Adult flukes buccal cavity and sophagus 1

SECOND INTERMEDIATE HOST

.Fish - of many species

Metacercariai stage encj. throughout body tissues

FIGURE 1. The life cycle of Clinostromum mar ' natum adapted from Hunter and Hunter 70E77 -5- Hunter and Hunter (1930) indicate that the infestation of yellow perch was highest in shallow, weedy water. Van Cleave and Mueller (1934) also found that C. marginatum was more prevalent in yellow perch from the shallow Wilber in Oneida Lake. Nigrelli (1936) noted that the orders of fish with the highest nutber of species infested were warmwater pond fishes. The fish hosts listed herein are primarily lacustrine fishes but there are several lotic fishes represented also. Intense parasitism of many stream fishes has occurred when these fish have been confined to lake or pond situations (Linton, 1911; Uzmann and Douglas, 1966). Infestations of fish confined strictly to stream habitats usually are not severe. Baker (1945) observed that snails of the genus Helisoma are littoral and are seldom found below 15 feet. This would indicate that cercariae to fish contact would be greatest in shallow littoral areas.

Most of the literature regarding C. marginatum has been restricted to fish parasite surveys. However, Klaas (1963) intensely studied some of the ecological factors associated with the occurrence of C. mEgIulLa in several ponds in eastern Kansas. He found no correlation between any environmental factor and the degree of parasit- tan,. Heavily infested fish populations existed in ponds where the incidence of infected snails was very low or where no snails were found. The production of cercariae by infected snails is such that a few infected snails could infect large numbers of fish (Edney, 1950). Fischthal (1953) discusses many of the ecological factors as they relate to parasitism of fishes. Factors which may be involved with C. marginatum infestations are water depth; thermal and chemical stratification; abundance-of weeds, snails and herons; fish behavior and habitat preference; population dynamics of snail populations (Edney, 1950; Klaas, 1963) and the physiological condition of the host to name a few.

Effects on Fish

Epizootics of C. marginatum have been reported for the-yelliow perch (Elliot and Russert, 1949; Van Cleave and Mueller, 1934),. black bullhead (Meyer, 1958; Forney, 1955), channel catfish (Edney, 1940), and steelhead trout (Uzmann and Douglas, 1966). Swartz (1956) observed the death of Noturus muirus in captivity and attributed death to. an infestation of C. mar inatum. Forney (1955) found INFES- TATIONS of the black bullhead in Clear—Lake, Iowa, which exceeded 500 cysts per fish. Young-of-the-year fish were found emaciated and dying in some areas of the lake.

Fish host specificity appears to be nearly nonexistent for this parasite. Klaas (1963) found the highest rate of infestation and the highest number of cysts per fish in the black bullhead. I have observed heavy infestation of the white catfish at Lower Otay Reservoir and the threadfin shad at El Capitan Reservoir in San Diego County, California. These high infestations appear to be related to extrinsic environmental factors since the same species may be lightly infested in other parts of the same body of water or in other waters.

The severe parasitism of steelhead trout reported by Uzmann and Douglas (1966) occurred in a lake which had been stocked with fingerling steelhead. The occurrence of C. marginatum in steelhead has been reported before only-by Haderlie (1953). This rare epizootic in the steelhead is Apparently . related-tO its confinement to a lacustrine environment favorable to fish to cercaria contact (Nigrelli, 1936).

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It is interesting to note that the carp has not been reported as a host for this parasite, although it has been examined in many fieh parasite surveys. This - species is common in lacustzine environs and is usually found in the shallow water .habitat of the snail vector.. Results of experimental infestation of carp would be interesting. The heavy scales of carp may be a barrier to penetration of the cercariae, whereas the lack of scales in members of the Family Ictaluridae may partially explain the occurrence of severe infestations in' that group.

Although Forney (1955) found black bullheads to be emaciated by C. marginatum, Elliot and Russert (1949) and Rabideau.and Self (1953) found no correlation between te parasite burden and con&ition factors of parasitized fish. However, Elliot 1 esert found that older, larger fish had a heavier parasite burden than Ty,tnger, smaller fish.

D):ly reports of Van Cleave and Mueller (1934) and Smallwood (1914) that fish lose their parasites during the winter in temperate climates, have been involidatei by studies of Fischthal (1949) which showed that overwinter loss of metazc:cariae fish is insignificant.

HOST OF CLINOSTOMUM MARGINATUM

Fish Hosts

A check list of fish hosts for the metacercarial:stage of C. marginatum nay'prove v: .7A to fishery. menegers, parasitologists, and researchers. An extensive s en ' e literature pertaining to this parasite in North America was made. Omissf. .8 list:or in the bibliography are the fault of the author. No attempt has Leen made to report fish hosts for this species outside North America.

C. marginatum occurs in 15 families and 67 species of freshwater and estuarine fishes. Nomenclature appearing in the original publications has been revised wherever possible to conform wi:th the American Fisheries Society's special publi- cation No. 24 A List of Common and Scientific Names of Fishes, second edition, (1960).

The number following each common name is the author reference: number appearing in the bibliography. The abbreviation SD refers to the occurrence of marginatum in San Diego County (data, unpublished)

Scientific Name Common Name Reference LepisOsteidae , Lepisostetja ple_ityrhincus DeKay Florida gar 6 Clupeidae Alosa sapidissima (Wilson) American shad 33 Dorosoma petenense (Giinther Tbreadfin shad SD Salmonidae Salmo Clarki Richardson Cutthroat trout 64 Salmo gairdneri Richardson. Rainbow trout 30, 64 Salvelinusjontinalis (Mitchill) Brook trout' 48, 50. UMbridae Umbra 'Jul (Kirtland) Central rintiminnow 24, 27 -7-

Scientific Name Common Name Reference 411•100

Esocidae Esox lucius Linnaeus X masquinow Hybrid 7 Mitchill Esox niger LeSueur Chain pickerel 6, 52, 61 Esox lucius Linnaeus Northern pike 24, 27, 49

Cyprinidae Campostomwn anomalum (Rafinesque) Stoneroller 24 26 Chrosomus eos Cope Northern tedbelly dace 7 Gila atraria (Girard) Utah chub 8 Hybopsis biguttata (Kirtland) Hornyhead chub 24 Mylocheilus caurinus (Richardson) Peamouth 13 Notemigonus crysoleueas (MITCHILL) Golden shiner 45 Notropis cornutus (Mit chill) Common shiner 5, 7, 121 24, 26 pimephales,notatus (Rafinesque) Bluntnose minnow 62 Pimephales Eromelas Rafinesque Fathead minnow 12, 45, 62, 65 Rhinichthys cataractae Longnose dace 24 • (ValencieTai)----- Rhinichthys osculus (Girard) Speckled dace 8 Richardsonius bilteatus Redside shiner 8,13

Semotilus atromaculatus (Mitchill) Creek chub 12, 24 26, 40 SEMOTILUS Corporalis (Mitchill) Fall fish 12

Catostomidae CatostOmus commersoni (Lac‘Ale) Common sucker 5, 24, 53, 65 Catostomus fecupius Cope and Yarrow Webug sucker 8 Catottomus humboldtianus (Snyder) Humboldt sucker 30 Catottomus rimiculus Gilbert and Klamath amallscale 30 Snyder sucker - Etimyzon sucena oblongus Chub sucker 11, 36 (MIT CHILL )1 Erimyzon oblongus (Mitchill) 'Creek chubsucker 61 Hypentelium nigricans (LeSueur) Northern hogsucker. 24 26 Moxostoma erythrurum (Rafinesque) Golden redhorse 24 MoxostomaValenciennesi Jordan Greater redhorse 27

Ictaluridae - IctalUrus catus (Linnaeus) White catfish 6, SD IctalUrus melas (Rafinesque) Black bullhead 10, 24, 29, 31, 35, 45, 51, SD Ictalurus natalis (LeSueur) Yellow bullhead 6, 24, 26, 57 . Ictalurus nebulosus (LeSueur) Brown bullhead 5, 9,.24, 26, 27, 30, 36, .40, 43., ' 52, 53, 62, SD /ctalurus punctatus (Rafinesque) Channel catfish 6, 11, 22A, 31, SD Notttrus flavus Rafinesque Stonecat 24 iMul-rusraiurus4 Jordan • Brindled madtom 60

'Nomenclature reported in the original paper. Synonymy not clear.

-8- Scientific Name Common blame Reference Cyprinodontidae Pundulus diaphanus (LeSueur) Banded killifish 7)52 Poeciliidae Mollienesia latipinna LeSueur Sailfin molly 6 Aphredoderidae Aphredoderus sayanus (Gilliams) Pirate perch 34 Serranidae Roccus americanas (Gmelin) White perch Roccus mississippiensis (Jordan Yellow bass 11 and Eigenmann) Roccus saxatilis (Waibaum) Striped bass 55 Centrarchidae Atbloplites rupestris (Rafinesque) Rock bass 7, 9; 10, 24, 25, 26, 27, 41, 49, 53,65 Chaenobryttus losus (Cuvier) Warmouth 4, 11, 55 Enneacanthus obesus (Girard) Banded sunfish 38 Lepomis aurita-(annaeus) Redbreast sunfish 53 Lepomis mapjAas Rafinesque Green sunfish 45, 53, 59, SD Lepomis B112R2Eas (Linnaeus) Pumpkinseed 2, 7, 9, 2Pi.1:1 18,24, 25, 26, 27, 36, 37, 41, 42,. 46, 61, 65 Lepomis humilis (Girard) Orangespotted sunfish 45, 51, 59 Lepomis macrochirus Rafinesque Bluegill 4, 5) 7, 19, 11, 24; 25, 26, 27 30, 45, 53, SD LEPOMIS macrochirus Rafinesque X Hybrid 55 L. cyanellus Rafinesque Lepomis microlophus (Gl(nther) Redear sunfish 4, 11 Lepotnis punctatus (Valenciennes) Spotted sunfish 11 Micropterus dolomieu Lac4Pede Smallmouth bass 2) 3, 5, 71 9) 10, 12, 14, 18, 20, 24, 36, 37, 38, 40, 41, 48, 49) 52, 53) 55) 57, 61 Micropterus punctulatus (Rafinesque) Spotted bass 14 Micropterus saImoides (Lacepede) Largemouth bass 2, 3, 4, 7, 11, 14, 24, 26, 27, 36, 45, 48, 53, 57, 61, 63, 65, 66, SD Pomoxis annularis Rafinesque White crappie 45 j)01D.Oxis nigromaCULATus (LeSueur) Black crappie 11

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Percidae Etheostoma caeruleum Storer Rainbow darter 24 Etheostoma flabeilare Rafinesque Fantail 'darter 10, 24 Etheostoma nigruiThafinesque Johnny darter 10, 24, 26, 57 Perca flavescens (Mitchill) Yellow perch 5, 7, 9, 12, 16, 18, 23, 24, 25, 26, 27, 36, 37, 39, 40, 41, 48, 49, 52, 53, 55, 57, 61, 65 Percina canrodes (Rafinesque) Logperch lo Stizostedion vitreum vitreum Walleye 7, 24, 26, 27, 41, Tatchill) SD Sciaenidae Aplodinotus grunniens Rafinesque Freshwater drum 11 Bird and Snail Hosts Hunter and Hunter (1935) lists several known definitive hosts reported by several investigators. Nearly all of these are wading birds.

The following list of definitive hosts includes those listed for C. complanatum and C. marginatum in North America although some other references are included. The names given in the literature have been updated and restricted to the species rather than subspecies lever. The number following each host refers to the reference in the bibliography.

Scientific Name Common Name Reference

Ardea herodias Linnaeus Great bLue heron 4, 43, 45, 49, 55, 65 Nytticorax ac:Lic_ors_a (Linnaeus Black crowned night 43, 54 heron Mycteria americana Linnaeus Wood ibis 43 Chlidonias nige7thinnaeus) Black tern 43 Sterna hirundo Linnaeus Common tern 43 Botaurus lentiginosus (Rackett) American bittern 43 Butorides viresceET(Linnaeus) Green heron 15 Ardeola ralloides 17 Larus argentatus Pontoppidan Herring cull 43 Phalacrocorax auritus (Lesson) Double crested 52, 54 cormorant

REPORTED SNAIL HOSTS.

Scientific Name Reference _____ Helisoma cappanulatum Say 1821 43 Helisoma antrosa Conrad 1834 43 Helisoma trivolvis Say 1817 4 Helisoma tenue (Phillipi) Dunker 1850

WProbable intermediate host in San Dierso County. -10-

CONTROL MEASURES

Possible methods of breaking the life cycle of C. marginatum are discussed by Klaas (1963). Elimination of submerged aquatic weeds is suggested as a means of limiting snails to the very edge of ponds and reducing contact with snails. How- ever, aquatic weed control to effectively control snails would be impractical on most bodies of water.

I have observed heavy infestations of threadfin shad by C. marginatum in El Capitan Reservoir, San Diego County, where aquatic weeds are not abundant. The reduction of parasitism by the elimination of aquatic weeds has yet to be tested.

The elimination of great blue heron populations is neither feasible nor desirable.

The elimination of the snail host is probably the most feasible means of breaking the life cycle. Uzmann and Douglas (1966) reported the successful elimination of Helisoma from a 23-acre lake using copper sulfate (.5 ppm as Cu++). They did not, however, recommend such treatments as a routine management practice because of the toxicity of copper sulfate to other aquatic organisms. Klaas (1963) discussed the use of molluscicides and some of the problems involved with their use. Mollusci- cides used under natural conditions may not eliminate the snail population and the biotic potential is such that these populations are rapidly reestablished. The introduction of a suitable predator or competitor of snails might effectively control but not eliminate the snails.

Alvault and Allison (1965) have shown that red-ear sunfish reduce the number of snails (thaa) in experimental ponds resulting in a reduction of parasitism of the bluegill by the streigeid trematode, Postho to_mum. minimum. Under natural conditions, however, the control of the snail hosts may not be sufficient to reduce parasitism since only a few infected snails are needed to produce numerous cercariae. Nonetheless this approach does appear to be worth further exploration.

BIBLIOGRAPHY

Reference No.

la American Fisheries Society. 1960. A list of common and scientific names of fishes from the United States and Canada. Special Publica- tion No. 2. 2nd ed. Waverly Press, Inc. Baltimore, Md. 102 p. lb Avault, James W., Jr., and Ray Allison. 1965. Experimental biological eottrol of 4 tromatode parasite of bluegill. Exp. Parasitol., 17 : 296-301. lc Baker Frank C. 1945. The molluscan family Planorbidap. Univ. of Press, Urbana, I:11. 530 p. 2 Bangham, Ralph V. 1936. Parasites other than cestodes in black bass of Ohio. Ohio Jour. Scii, 26 (3) : 117-127. 3 - - . 1933. Parasites of the spotted bass Micropterus pasudsatyA Hubbs, and summary of parasites of smallmouth and largemouth black bass from Ohio streams. Trans. Amer. Fish. Soc., 63 : 220-277. 4 - - . 1938. Parasites of Centrarchidae from southern Florida, Trans. Amer. Fish. Soc., 68 : 263-368. 5 - - . 1940. Parasites of fish of Algonquin Park Lakes. Trans. - Amer.. Ptah. Soc., 70 : 161-171. -11-

Reference No.

6 - - . 1940. Parasites of freshwater fish of southern Florida. Proc. Fla. Acad. SO.., 5 : 289 - 307. 7 1944. :Parasites of northern Wisconsin fish. Trans. Wisc. Acad.. Sci., 36 : 291=325. 8 - - . 1951. 'Parasites of.fish of the Upper Snake River drainage and in Yellowstone Lake, Wyoming. Zoologiea, 36 (3) : 213-217. 9 - - . 1955. 'Studies on fishparasites of Lake Huron and Manitoulin Island. Amer. Midl. Nati, 53 (1) : 184-194. Bangham, Ralph V., and George W. Hunter III. 1939. Studies on fish parasites:of Lake. Erie.- Dietribution studies. Zoologica, 24 : 385-448. Bangham,. Ralph V.„ and C. E. Vtnard. , 1942. Studies on the parasites of Reelfoot Lake fish. . IV. Distribution studies. and check list. Tenn. Acad. SCi., 17 : 22.738. - 12 Bangham, Ralph V., and Carl E. Nenard. 1946. Parasites: of fish on : Algonquin Park Lakes. II. Distribution studies. Univ. Toronto Studies Biol., 53 : 33-46.. Bangham, Ralph V., and 'Yates R. Adams. .1954.- A survey of the parasites of freshwater fishes from the mainland of British' Columbia. Jour. Fish. Res. Bd. Canada, 11 : 673-708. Becker, David A., Robert G. Heard, and Perry Don Holmes. 1966. A pre-impoundment-survey of the helminth and copepod parasites of Micropterus app. Of Beaver Reservoir in northeast Arkansas. Trans. Arr. Fish. Soc., 95 (1) : 23-34. 15 Cabellero y, C. E. :1.946. Helminthological studies in the onehocerciasis region of 'Mexico and Guatemala. Trematoda II. Presence of Pe.14gonimus in natural reservoir hosts and description of a new genus. Univ. Nacion. Mexico, 17 (A) : 137-165. In Biol. Abet., 22 (1) : 2422. 16 Chandler, Asa C. 1951.' : Studies on the metacercariae of Perca flavescens in Lake Itasca, Minnesota. Amer. Midi. Nat., 45 (3) : 711-721. 17' Chapham, Phyllis A. .1945. Some helminthes from West Africa. Jour. .Helminthol., 21 (2/3) : 90-92. 18 Cooper, A. R. 1915. Trenatodes from Marine and freshwater. fishes including one species of ectoParasitic Tutbellarian. Trans. Roy. Soc. Canada, 9 (3) : 181-205. , • - 19 .Cort, W. W., D. J..Ame11, and.A. Van de Woude. 1950. Germinal material in the redise of Clinostotutiarginatum (Rudolphi). Jour. Parasitol., 36 (2) : 157-163. 20 Cross, S. X. 1938. A study of the fish parasite relationships in the Trout Lake region of Wisconsin., Trans. Wisc. Acad. Sc., 31 : 439-456. 21; Davis, H. S. 1953.. Culture and'diseaees of game fishes.' Univ. Calif. Press, Berkeley and L'14.Arigeles. ,332 p. . . • 22a. Edney, J. N. :1940. A heavy infestation of Clinostomum niarginatum metacerdarie in chap:1cl Catfish. ' Jour. Tenn. Acad. Sci., 15 4) : 371. , . • • - , 22b. . 1950. PrOducti7ity in.Clinostomum:marginatuM. Trans. Amer. Micro. Soc., 69 : 186-186. -12- Reference No. 23 Elliot, A. M., and L. R. Russert. 1949. Some condition characteristics of a yellow perch population heavily parasitized by Clinostomum narginatum. Jour. Parasitol., 35 (2) : 183-190. 24 Fischthal, J. H. 1947. Parasites of northwest Wisconsin fishes. I. The 1944 survey. Trans. Wisc. Acad. Sc., 37 : 157-220. 25 - - . 1949. The over-wintering of black and yellow grubs in fish. Jour. Parasitol., 35 : 191-192. 26 - - . 1950. Parasites of northwest Wisconsin fishes. II. The 1945 survey. Trans. Wisc. Acad. Sc., 40 : 87-113. 27 - - 4 1952. Parasites of northwest Wisconsin fishes. III. The 1946 survey. Trans. Wisc. Acad. Sc., 41 : 17-58. 28 - - . 1953. Parasites of northwest Wisconsin fishes. IV. Summary and limnological relationships. Trans. Wisc. Acad. Sc., 42 : 83-108. 29 Forney, J. L. 1955. Life history of the black bullhead Ameirus nelas (Rafinesque), of Clear Lake, Iowa. Iowa St. Coll* Jour. Sci.,7571) : 145-162. 30 Haderlie, Eugene Clinton. 1953. Parasites of the freshwater fiabes of northern California. Univ. Calif. Publ. Zool., 57 (5) : 303-440. 31 Harms, C. E. 1959. Checklist of parasites from catfishes of northeastern Kansas. Kans. Acad. Sc., 62 (4) : 262. 32 Hemenway, Marilyn. 1948. Studies on encystment of Clinostomum marginatum by use of artificial digest. Iowa Acad. Sc,, 55 : 375-377 33 Hollis, E. H., and C. M. Coker. 1948. A trematode parasite of the genus Clinostomum new to the shad, Alosa sapidissima. Jour. Parasitol., 34 (6) 77.53-495. 34 Hopkins, S. H. 1933. Note on the life history of Clinostomum marginatum (Trematoda). Trans. Amer. Micro. Soc., 52 (2) : 147-149. 35 Hugghins, Ernest J. 1959. Parasites of fishes of South Dakota. So. Dakota Agr. Ext., Sta. Bull, 484, 72 p. 36 Hunninen, A. V. 1936. Studies of fish parasites in the Delaware and SusquehArnA watersheds, p. 237-245. In A biological survey of the Delaware and Susquehanna watersheds. New York Cons. Dept., Suppl. to 25th Ann. Rept. (1935), 37 Hunter, George W. III. 1942. Studies on the parasites of freshwater fishes of Connecticut. A fishery survey of important Connecticut lakes. Conn. Geol. and Nat. Hist. Surv. Bull., (62) : 228-288. 38 Hunter, George W. III, and H. Clark Dalton. 1939. Studies on Clinostomum. V. The cysts of the yellow grub of fish (Clinostomum narginatum). Proc. Helminthol. Soc. Wash., 6 (2) : 73-76. 39. Hunter, George W. III, and Wanda S. Hunter. 1930. Studies on the parasites of fishes on the Lake Champlain watershed, p. 241-260. In A biological survey of the Lake Champlain watershed. New York Cons. Dept., Suppl. to 19th Ann. Rept. (1929). 40 - - . 1931. Studies of fish parasites in the St. Lawrence watershed, p. 197-216. In A biological survey of the St. Lawrence watershed. New York Cons. Dept., Suppl. to 20th Ann. Rept. (1930). - . 1932. X. Studies on parasites of fish and fish eating birds, p. 252-271. In A biological survey of the Oswegatchie and Black River systems. New York Cons. Dept., Suppl. to 21st Ann. Rept. (1931). -13- Reference No.

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